Transgressivity in key functional traits rather than phenotypic plasticity promotes stress tolerance in a hybrid cordgrass

Authors: GALLEGO-TEVAR, BLANCA - University Of Seville; Grewell, Brenda; DRENOVSKY, REBECCA - John Carroll University; CASTILLO, JESUS - University Of Seville

Submitted to: Plants
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 12/3/2019
Publication Date: 12/12/2019
Citation: Gallego-Tevar, B., Grewell, B.J., Drenovsky, R.E., Castillo, J.M. 2019. Transgressivity in key functional traits rather than phenotypic plasticity promotes stress tolerance in a hybrid cordgrass. Plants. 8(12):594. https://doi.org/10.3390/plants8120594.
DOI: https://doi.org/10.3390/plants8120594

Interpretive Summary: Hybridization between plant species can increase genetic diversity upon with natural selection can act, and may increase the invasiveness of alien species. The hybridization process may also increase the success of colonization in novel environments by overcoming low genetic diversity otherwise associated with founder effects. A lack of understanding of the mechanisms underlying hybridization and ecological impacts of hybrid taxa limits our ability to control the biological invasions by aggressive hybrids. Improved understanding of the hybrid invasion process is crucial for developing effective intergrated management strategies. Hybridization may promote offspring fitness via greater tolerance to environmental stressors due to heterosis, the superior tendency of a cross-bred plant to show functional traits that are superior to both parental species. This enhanced performance could also be due to higher levels of phenotypic plasticity of key traits influencing plant growth. Analyzing phenotypic inheritance of hybrids provides an opportunity to elucidate further plant responses to environmental stress. In the case of coastal salt marshes, sea level rise associated with climate change will subject hybrids, and their parental species, to longer periods of tidal submergence and higher aqueous and sediment salinity. We analyzed phenotypic inheritance expression patterns in the hybrid Spartina densiflora x foliosa relative to its parental species, native S. foliosa and invasive S. densiflora, from the San Francisco Estuary (California, USA) when exposed to contrasting salinity and inundation levels in a mesocosm experiment. The hybrid expressed 36% of co-dominant traits from both parents, 26% transgressive traits, and 17% traits dominantly from one of the parental species, whereas only 3% of response traits were intermediate between both parents. Thus, transgressivity rather than phenotypic plasticity in key functional traits of the hybrid, such as tiller height, conveyed greater stress tolerance to the hybrid compared to tolerance of its parents. As parental trait variability increased, phenotypic transgressivity of the hybrid increased and was more important in response to inundation stress than salt stress. The adaptive evolutionary process of hybridization is thought to support increased invasiveness of plant species and their rapid evolution. Our findings suggest increases in salinity and inundation associated with sea level rise will amplify the superiority of the transgressive hybrid S. densiflora x foliosa over its parental species. These results provide evidence of transgressive traits as an underlying source of adaptive variation that can facilitate the establishment of invasive plants in new and changing environments.

Technical Abstract: Hybridization may promote offspring fitness via greater tolerance to environmental stressors due to heterosis and/or higher levels of phenotypic plasticity. Thus, analyzing phenotypic inheritance of hybrids provides an opportunity to elucidate further plant responses to environmental stress. In the case of coastal salt marshes, sea level rise associated with climate change will subject hybrids, and their parental species, to longer periods of tidal submergence and higher aqueous and sediment salinity. We analyzed phenotypic inheritance expression patterns in the hybrid Spartina densiflora x foliosa relative to its parental species, native S. foliosa and invasive S. densiflora, from the San Francisco Estuary (California, USA) when exposed to contrasting salinity and inundation levels in a mesocosm experiment. The hybrid expressed 36% of co-dominant traits from both parents, 26% transgressive traits, and 17% traits dominantly from one of the parental species, whereas only 3% of response traits were intermediate between both parents. Thus, transgressivity rather than phenotypic plasticity in key functional traits of the hybrid, such as tiller height, conveyed greater stress tolerance to the hybrid compared to tolerance of its parents. As parental trait variability increased, phenotypic transgressivity of the hybrid increased and was more important in response to inundation stress than salt stress. The adaptive evolutionary process of hybridization is thought to support increased invasiveness of plant species and their rapid evolution. Our findings suggest increases in salinity and inundation associated with sea level rise will amplify the superiority of the transgressive hybrid S. densiflora x foliosa over its parental species. These results provide evidence of transgressive traits as an underlying source of adaptive variation that can facilitate the establishment of invasive plants in new and changing environments.